Changes in the regulatory effects of cell-cell interactions on neuronal AChR subunit transcript levels after synapse formation

Journal of Neuroscience

Volumn 16, Issue 21, 1996, Pages 6878-6885

  Levey, Marjory S ^a   Jacob, Michele H ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

axotomy; denervation; development; mRNA; nicotinic acetylcholine receptors (AChRs); parasympathetic ciliary ganglion neurons; regulation of gene expression; synapse formation and maturation

Indexed keywords

CHOLINERGIC RECEPTOR; COLCHICINE; NICOTINIC RECEPTOR; RECEPTOR SUBUNIT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CHOLINERGIC SYSTEM; CILIARY GANGLION; CONTROLLED STUDY; EMBRYO; NERVE CONDUCTION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS;

EID: 0029960522     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-21-06878.1996     Document Type: Article

References (48)

1. Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
2. Anand R, Conroy WG, Schoepfer R, Whiting P, Lindstrom J (1991) Neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes have a pentameric quaternary structure. J Biol Chem 266:11192-11198.
3. Arenella LS, Oliva JM, Jacob MH (1993) Reduced levels of acetylcholine receptor expression in chick ciliary ganglion neurons developing in the absence of innervation. J Neurosci 13:4525-4537.
4. Bodian D, Mellors RC (1945) The regenerative cycle of motoneurons, with special reference to phosphatase activity. J Exp Med 81:469-488.
5. Boyd RT, Jacob MH, Couturier S, Ballivet M, Berg DK (1988) Expression and regulation of neuronal acetylcholine receptor mRNA in chick ciliary ganglia. Neuron 1:495-502.
6. Brenner HR, Johnson EW (1976) Physiological and morphological effects of post-ganglionic axotomy on presynaptic nerve terminals. J Physiol (Lond) 260:143-158.
7. Brenner HR, Martin AR (1976) Reduction in acetylcholine sensitivity of axotomized ciliary ganglion cells. J Physiol (Lond) 260:159-175.
8. Conroy WG, Berg DK (1995) Neurons can maintain multiple classes of nicotinic acetylcholine receptors distinguished by different subunit compositions. J Biol Chem 270:4424-4431.
9. Cooper E, Couturier S, Ballivet M (1991) Pentameric structure and subunit stoichiometry of a neuronal nicotinic acetylcholine receptor. Nature 350:235-238.
10. Corriveau RA, Berg DK (1993) Coexpression of multiple acetylcholine receptor genes in neurons: quantification of transcripts during development. J Neurosci 13:2662-2671.
11. Couturier S, Erkman L, Valera S, Rungger D, Bertrand S, Boulter J, Ballivet M, Bertrand D (1990) α5, α3, and non-α3: three clustered avian genes encoding neuronal nicotinic acetylcholine receptor-related subunits. J Biol Chem 265:17560-17567.
12. Darland DC, Link BA, Nishi R (1995) Activin A and follistatin expression in developing targets of ciliary ganglion neurons suggests a role in regulating neurotransmitter phenotype. Neuron 15:857-866.
13. Davis RE (1990) Effect of optic nerve lesions and intraocular colchicine on cell proliferation in the germinal zone of the optic tectum and in the torus longitudinalis in the goldfish. Brain Res 512:46-53.
14. 2+/calmodulin-dependent kinase pathway. J Neurosci 15:7966-7978.
15. + currents in chick ciliary ganglion neurons developing in situ. J Neurosci 14:3156-3165.
16. Feramisco JR, Smart JE, Burridge K, Helfman DM, Thomas GP (1982) Co-existence of vinculin and a vinculin-like protein of higher molecular weight in smooth muscle. J Biol Chem 257:11024-11031.
17. Finn TP, Nishi R (1996) Expression of a chicken ciliary neurotrophic factor in targets of ciliary ganglion neurons during and after the cell-death phase. J Comp Neurol 366:559-571.
18. Furber S, Oppenheim RW, Prevette D (1987) Naturally occurring neuron death in the ciliary ganglion of the chick embryo following removal of preganglionic input: evidence for the role of afferents in ganglion cell survival. J Neurosci 7:1816-1832.
19. Grant MP, Francis NJ, Landis SC (1995) The role of acetylcholine in regulating secretory responsiveness in rat sweat glands. Mol Cell Neurosci 6:32-42.
20. Habecker BA, Landis SC (1994) Noradrenergic regulation of cholinergic differentiation. Science 264:1602-1604.
21. Habecker BA, Tresser SJ, Rao MS, Landis SC (1995) Production of sweat gland cholinergic differentiation factor depends on innervation. Dev Biol 167:307-316.
22. Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49-82.
23. Hieber V, Agranoff BW, Goldman D (1992) Target-dependent regulation of retinal nicotinic acetylcholine receptor and tubulin RNAs during optic nerve regeneration in goldfish. J Neurochem 58:1009-1015.
24. Jacob MH (1991) Acetylcholine receptor expression in developing chick ciliary ganglion neurons. J Neurosci 11:1701-1712.
25. Jacob MH, Berg DK (1987) Effects of preganglionic denervation and postganglionic axotomy on acetylcholine receptors in the chick ciliary ganglion. J Cell Biol 105:1847-1854.
26. Jacob MH, Berg DK (1988) The distribution of acetylcholine receptors in chick ciliary ganglion neurons following disruption of ganglionic connections. J Neurosci 8:3838-3849.
27. Karlsson J-O, Sjostrand J (1969) The effect of colchicine on the axonal transport of protein in the optic nerve and tract of the rabbit. Brain Res 13:617-619.
28. Landmesser L, Pilar G (1972) The onset and development of transmission in the chick ciliary ganglion. J Physiol (Lond) 222:691-713.
29. Landmesser L, Pilar G (1974a) Synapse formation during embryogenesis on ganglion cells lacking a periphery. J Physiol (Lond) 241:715-736.
30. Landmesser L, Pilar G (1974b) Synaptic transmission and cell death during normal ganglionic development. J Physiol (Lond) 241:737-749.
31. Levey MS, Brumwell CL, Dryer SE, Jacob MH (1995) Innervation and target tissue interactions differentially regulate acetylcholine receptor subunit mRNA levels in developing neurons in situ. Neuron 14:153-162.
32. Listerud M, Brussaard AB, Devay P, Colman DR, Role LW (1991) Functional contribution of neuronal AChR subunits revealed by antisense oligonucleotides. Science 254:1518-1521.
33. Mandelzys A, Pie B, Deneris ES, Cooper E (1994) The developmental increase in ACh current densities on rat sympathetic neurons correlates with changes in nicotinic ACh receptor α-subunit gene expression and occurs independent of innervation. J Neurosci 14:2357-2364.
34. Margiotta JF, Gurantz D (1989) Changes in the number, function, and regulation of nicotinic acetylcholine receptors during neuronal development. Dev Biol 135:326-339.
35. Martin AR, Pilar G (1963a) Dual mode of synaptic transmission in the avian ciliary ganglion. J Physiol (Lond) 168:443-463.
36. Martin AR, Pilar G (1963b) Transmission through the ciliary ganglion of the chick. J Physiol (Lond) 168:464-475.
37. McEachern AE, Jacob MH, Berg DK (1989) Differential effects of nerve transection on the ACh and GABA receptors of chick ciliary ganglion neurons. J Neurosci 9:3899-3907.
38. Meriney SD, Pilar G (1987) Cholinergic innervation of the smooth muscle cells in the choroid coat of the chick eye and its development. J Neurosci 7:3827-3839.
39. Perisic M, Cuenod M (1972) Synaptic transmission depressed by colchicine blockade of axoplasmic flow. Science 175:1140-1142.
40. Pilar G, Landmesser L (1972) Axotomy mimicked by localized colchicine application. Science 177:1116-1118.
41. Pilar G, Nunez R, McLennan IS, Meriney SD (1987) Muscarinic and nicotinic synaptic activation of the developing chicken iris. J Neurosci 7:3813-3826.
42. Ramirez-Latorre J, Yu CR, Ou X, Perin F, Karlin A, Role L (1996) Functional contributions of α5 subunit to neuronal acetylcholine receptor channels. Nature 380:347-351.
43. Role LW (1988) Neural regulation of acetylcholine sensitivity in embryonic sympathetic neurons. Proc Natl Acad Sci USA 85:2825-2829.
44. Smith MA, Stollberg J, Lindstrom JM, Berg DK (1985) Characterization of a component in chick ciliary ganglia that cross-reacts with monoclonal antibodies to muscle and electric organ acetylcholine receptor. J Neurosci 5:2726-2731.
45. Sullivan KF, Havercroft JC, Machlin PS, Cleveland DW (1986) Sequence and expression of the chicken β5 and β4-tubulin genes define a pair of divergent β-tubulins with complementary patterns of expression. Mol Cell Biol 6:4409-4418.
46. Thomas WS, Jacob MH, O'Dowd DK, Smith MA (1995) Agrin gene expression in ciliary ganglion neurons following preganglionic denervation and postganglionic axotomy. Dev Biol 168:662-669.
47. Vernallis AB, Conroy WG, Berg DK (1993) Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaining subunit segregation among receptor subtypes. Neuron 10:451-464.
48. Yu C, Brussaard AB, Yang X, Listerud M, Role LW (1993) Uptake of antisense oligonucleotides and functional block of acetylcholine receptor subunit gene expression in primary embryonic neurons. Dev Genet 14:296-304.